TY - JOUR

T1 - Genomes of the Venus Flytrap and Close Relatives Unveil the Roots of Plant Carnivory

AU - Palfalvi, Gergo

AU - Hackl, Thomas

AU - Terhoeven, Niklas

AU - Shibata, Tomoko F.

AU - Nishiyama, Tomoaki

AU - Ankenbrand, Markus

AU - Becker, Dirk

AU - Förster, Frank

AU - Freund, Matthias

AU - Iosip, Anda

AU - Kreuzer, Ines

AU - Saul, Franziska

AU - Kamida, Chiharu

AU - Fukushima, Kenji

AU - Shigenobu, Shuji

AU - Tamada, Yosuke

AU - Adamec, Lubomir

AU - Hoshi, Yoshikazu

AU - Ueda, Kunihiko

AU - Winkelmann, Traud

AU - Fuchs, Jörg

AU - Schubert, Ingo

AU - Schwacke, Rainer

AU - Al-Rasheid, Khaled

AU - Schultz, Jörg

AU - Hasebe, Mitsuyasu

AU - Hedrich, Rainer

N1 - Funding information: This work was supported by the European Research Council (ERC) under the EU 7th Framework Program ( FP/20010- 2015 )/ERC grant agreement 250194 Carnivorom to R.H., by a DFG -funded Reinhart Koselleck project ( HE 1640/42-1 ; project number 415282803 ) to R.H., by a JSPS KAKENHI grant ( 22128008 to T.N. and 22128001 , 22128002 , 16H06378 , and 17H06390 to M.H.), and by a Researchers Supporting Project ( NSRSP-2019 ), King Saud University , Riyadh, Saudi Arabia to K.A.-R. and R.H. C.K. was supported by the RA program of National Institute for Basic Biology . Dr. spatulata cultivation, genome sequence, and computer analyses were partly supported by MPRF-NIBB , DIAF-NIBB , and ROIS National Institute of Genetics . The ORCIDs for the authors are as follows: https://orcid.org/0000-0002-0838-7700 (J.S.), https://orcid.org/0000-0001-7425-8758 (M.H.), and https://orcid.org/0000-0003-3224-1362 (R.H.). This work was supported by the European Research Council (ERC) under the EU 7th Framework Program (FP/20010- 2015)/ERC grant agreement 250194 Carnivorom to R.H. by a DFG-funded Reinhart Koselleck project (HE 1640/42-1; project number 415282803) to R.H. by a JSPS KAKENHI grant (22128008 to T.N. and 22128001, 22128002, 16H06378, and 17H06390 to M.H.), and by a Researchers Supporting Project (NSRSP-2019), King Saud University, Riyadh, Saudi Arabia to K.A.-R. and R.H. C.K. was supported by the RA program of National Institute for Basic Biology. Dr. spatulata cultivation, genome sequence, and computer analyses were partly supported by MPRF-NIBB, DIAF-NIBB, and ROIS National Institute of Genetics. The ORCIDs for the authors are as follows: https://orcid.org/0000-0002-0838-7700 (J.S.), https://orcid.org/0000-0001-7425-8758 (M.H.), and https://orcid.org/0000-0003-3224-1362 (R.H.). Y.H. and K.U. provided aseptic culture of Dr. spatulata. C.K. and K.F. maintained and collected Dr. spatulata samples and extracted DNA. T.F.S. T.N. S.S. and Y.T. performed genome sequencing of Dr. spatulata. L.A. cultured and provided A. vesiculosa plants. I.K. maintained aseptic cultures and extracted DNA for A. vesiculosa and Di. muscipula. T.W. established and provided aseptic cultures and determined genome size of Di. muscipula and A. vesiculosa. J.F. determined Di. muscipula genome size. G.P. T.F.S. T.N. and S.S. assembled and annotated Dr. spatulata genome. T.H. F.F. and M.A. developed and T.H. implemented the assembly strategy for the Di. muscipula genome. N.T. assembled A. vesiculosa genome, and G.P. and N.T. annotated all three species. G.P. identified WGDs, analyzed syntenic regions, identified and analyzed expanded and contracted gene families, designed figures, and performed comparison with N. alata. N.T. developed strategy for LTR identification, D.B. analyzed expanded protein families, F.S. performed tissue-specific gene analysis and performed orthogroup analyses, and M.F. analyzed composition and age of LTRs, performed TF binding site analysis, and analyzed A. thaliana orthologs of carnivory-specific genes. A.I. analyzed genome data and designed figures, I.S. analyzed genome data, and R.S. performed membrane protein classification. J.S. designed and directed computational analyses. G.P. J.S. M.H. R.H. and K.A.-R. wrote the paper with input from all authors. M.H. and R.H. devised the project. J.S. M.H. and R.H. are representatives of each group. G.P. and T.H. should be considered joint first authors. The authors declare no competing interests.

PY - 2020/6/22

Y1 - 2020/6/22

N2 - Most plants grow and develop by taking up nutrients from the soil while continuously under threat from foraging animals. Carnivorous plants have turned the tables by capturing and consuming nutrient-rich animal prey, enabling them to thrive in nutrient-poor soil. To better understand the evolution of botanical carnivory, we compared the draft genome of the Venus flytrap (Dionaea muscipula) with that of its aquatic sister, the waterwheel plant Aldrovanda vesiculosa, and the sundew Drosera spatulata. We identified an early whole-genome duplication in the family as source for carnivory-associated genes. Recruitment of genes to the trap from the root especially was a major mechanism in the evolution of carnivory, supported by family-specific duplications. Still, these genomes belong to the gene poorest land plants sequenced thus far, suggesting reduction of selective pressure on different processes, including non-carnivorous nutrient acquisition. Our results show how non-carnivorous plants evolved into the most skillful green hunters on the planet.

AB - Most plants grow and develop by taking up nutrients from the soil while continuously under threat from foraging animals. Carnivorous plants have turned the tables by capturing and consuming nutrient-rich animal prey, enabling them to thrive in nutrient-poor soil. To better understand the evolution of botanical carnivory, we compared the draft genome of the Venus flytrap (Dionaea muscipula) with that of its aquatic sister, the waterwheel plant Aldrovanda vesiculosa, and the sundew Drosera spatulata. We identified an early whole-genome duplication in the family as source for carnivory-associated genes. Recruitment of genes to the trap from the root especially was a major mechanism in the evolution of carnivory, supported by family-specific duplications. Still, these genomes belong to the gene poorest land plants sequenced thus far, suggesting reduction of selective pressure on different processes, including non-carnivorous nutrient acquisition. Our results show how non-carnivorous plants evolved into the most skillful green hunters on the planet.

KW - Droseraceae

KW - gene loss

KW - jasmonate signaling

KW - neofunctionalization

KW - tissue-specific genes

KW - transposon classification

KW - whole-genome duplications

KW - WRKY transcription factors

UR - http://www.scopus.com/inward/record.url?scp=85085305529&partnerID=8YFLogxK

U2 - 10.1016/j.cub.2020.04.051

DO - 10.1016/j.cub.2020.04.051

M3 - Article

C2 - 32413308

AN - SCOPUS:85085305529

VL - 30

SP - 2312-2320.e5

JO - Current Biology

JF - Current Biology

SN - 0960-9822

IS - 12

ER -